Effects of Introduced Mosquitofish and Bullfrogs on the Threatened California Red-Legged Frog SHARON P. LAWLER,*‡ DEBORAH DRITZ,* TERRY STRANGE,† AND MARCEL HOLYOAK* *Department of Entomology, University of California, Davis, CA 95616–8584, U.S.A. †San Joaquin County Mosquito and Vector Control District, 7759 South Airport Way, Stockton, CA 95206, U.S.A. Abstract: Exotic species have frequently caused declines of native fauna and may contribute to some cases of amphibian decline. Introductions of mosquitofish (Gambusia affinis) and bullfrogs (Rana catesbeiana) are suspected to have caused the decline of California red-legged frogs (Rana aurora draytonii). We tested the ef- fects of mosquitofish and bullfrog tadpoles on red-legged frog tadpoles in spatially complex, speciose commu- nities. We added 720 hatchling red-legged frog tadpoles to each of 12 earthen ponds. Three ponds were con- trols, 3 were stocked with 50 bullfrog tadpoles, 3 with 8 adult mosquitofish, and 3 with 50 bullfrogs plus 8 mosquitofish. We performed tests in aquaria to determine whether red-legged frog tadpoles are preferred prey of mosquitofish. Mosquitofish fed on a mixture of equal numbers of tadpoles and either mosquitoes, Daphnia, or corixids until , 50% of prey were eaten; then we calculated whether there was disproportionate predation on tadpoles. We also recorded the activity of tadpoles in the presence and absence of mosquitofish to test whether mosquitofish interfere with tadpole foraging. Survival of red-legged frogs in the presence of bullfrog tadpoles was less than 5%; survival was 34% in control ponds. Mosquitofish did not affect red-legged frog sur- vival, even though fish became abundant (approximately 1011 per pond). Two mechanisms may have blocked the effects of mosquitofish on tadpole survival: (1) fish ponds contained fewer predatory inverte- brates, and (2) mosquitofish preferred other prey to red-legged frogs in laboratory trials. Red-legged frog tad- poles suffered more injuries in ponds with fish, however, and weighed 34% less at metamorphosis. The growth decrease could have been caused by injuries or by lower foraging levels in the presence of fish. Labo- ratory results showed that young tadpoles were less active in the presence of mosquitofish. Although both mosquitofish and bullfrogs affected red-legged frogs, the impact of bullfrogs on the survival of red-legged frogs may contribute more strongly to their decline. Effectos de la Introducción del Pez Mosquito y Rana Toro en Poblaciones de la Rana Resumen: Especies exóticas han ocasionado frecuentemente disminuciones de fauna nativa y pueden con- tribuir en algunos casos a la disminución de anfibios. Introducciones del pez mosquito (Gambusia affinis) y rana toro ( Rana catesbeiana) son consideradas como la causa del declive de la rana patiroja de California ( Rana aurora draytonii). Evaluamos los efectos del pez mosquito y renacuajos de rana toro en renacuajos de rana patiroja en comunidades espacialmente complejas. Agregamos 720 renacuajos recién eclosionados a cada uno de los 12 estanques de tierra. Tres de los estanques eran controles, tres fueron sembrados con 50 renacuajos de rana toro, tres con 8 adultos de pez mosquito y 3 con 50 renacuajos de rana toro mas ocho peces mosquito. Realizamos pruebas en acuarios para checar si los renacuajos de patiroja eran la presa preferida del pez mosquito. Los peces mosquito se alimentaron de una mezcla de igual número de renacua- jos y tanto mosquitos, Daphnias, o coríxidos, evaluamos si hubo una depredación desproporcionada de ren- acuajos una vez que alrededor del 50% de las presas fué comido. También observamos la actividad de los renacuajos en presencia y ausencia de peces mosquito para determinar si los peces interferían con el forra- jeo de los renacuajos. La supervivencia de ranas patiroja en presencia de renacuajos de rana toro fue redu- ‡email [email protected] Paper submitted February 20, 1998; revised manuscript accepted August 26, 1998. 613 Conservation Biology, Pages 613–622 Volume 13, No. 3, June 1999 614 Effects of Alien Species on Red-Legged Frogs Lawler et al. cida en un 5%; la supervivencia en los estanques control fué de un 34%. El pez mosquito no afectó la super- vivencia de la rana patiroja, aún cuando la abundancia de peces se tornó elevada (z1011 por estanque). Dos mecanismos pueden haber bloqueado los efectos del pez mosquito en la supervivencia de renacuajos: (1) los estanques con peces tuvieron menos invertebrados depredadores y (2) los peces mosquito prefírieron otro tipo de presas en los experimentos de laboratorio. Sin embargo, los renacuajos de rana patiroja sufrieron mas lesiones en estanques con peces y pesaron 34% menos durante metamorfósis. La disminución en crec- imiento pudo haber sido causada por lesines o por niveles mas bajos de forrajeo en presencia de peces. Los resultados de laboratorio muestran que los renacuajo jóvenes fueron menos activos en presencia de peces mosquito. A pesar de que tanto los peces mosquito como la rana toro afectaron a la rana patiroja, el impacto de la rana toro en la supervivencia de la rana patiroja contribuye mas fuertemente a su disminución. Introduction In a field survey of sites where red-legged frogs have bred historically, Hayes and Jennings (1986) found a Introduced species have caused declines or extinctions strong negative correlation between extant populations of native species worldwide. Some of the most ecologi- of the frog and the presence of introduced fish and bull- cally destructive introductions have been those in which frogs. We measured how tadpoles of red-legged frogs the alien species is a vertebrate that was introduced for are affected by bullfrogs and mosquitofish (Gambusia economic reasons (Williamson 1996) or when a general- affinis affinis). We selected the mosquitofish because ist predator is introduced as a biological control agent of its widespread and ongoing introduction (Rupp (Howarth 1991; Simberloff & Stiling 1996). Species are 1996); other species of fish may also play a role in the rarely introduced singly or in the absence of other decline of red-legged frogs. changes, such as habitat destruction, and this can make Bullfrogs are native to the eastern United States. They it difficult to relate the decline of a native species to the were introduced in the west to improve the frog “fishery” introduction of a particular alien species (Williamson and have been introduced to Europe as well (Stumpel 1996). Experimental work is necessary to estimate the 1992). Bullfrog tadpoles can be strong competitors effects of any one factor, preferably by manipulating one (Werner 1994; Kupferberg 1995). Red-legged frog tad- or more species independently under conditions that poles face competition from large, overwintering bull- are as natural as possible. We present a field experiment frog tadpoles because bullfrogs breed in summer and that quantified the effects of two introduced vertebrate red-legged frogs breed from January to March. Larger species on tadpoles of an endangered frog. tadpoles sometimes enjoy a greater per-capita competi- Non-native vertebrate species are suspected to have tive advantage (Lawler & Morin 1993; Werner 1994; contributed to the decline of the California red-legged Kupferberg 1995; Peacor & Werner 1997). In addition, frog (Rana aurora draytonii), which is listed as a threat- bullfrog tadpoles may consume northern red-legged frog ened species. The decline of this formerly abundant spe- tadpoles (Rana aurora aurora) under some circum- cies is one of the most dramatic examples of amphibian stances (Kiesecker & Blaustein 1997). The effects of decline (A. R. Blaustein et al. 1994), and examining causes bullfrog adults on native frogs may be even more pro- for this phenomenon could provide clues that may to aid nounced because bullfrogs will consume other frogs. Ex- in the recovery of other declining amphibians. Histori- perimental studies are needed to determine the effect of cally, R. a. draytonii bred throughout the lower central bullfrogs on other amphibians because several studies valley of California and in low elevations in the Sierra and have documented the decline of native species after coastal ranges, but it is now restricted largely to the bullfrog introductions (Kiesecker & Blaustein 1997). coastal foothills ( Jennings & Hayes 1985; Fisher & Shaffer Mosquitofish are native to the eastern United States, 1996). A dramatic early decline began in 1895 and was as- and have been introduced to wetlands worldwide as bio- sociated with human consumption of frogs, but the con- logical control agents for mosquito larvae. The practice of tinued loss of populations is poorly understood ( Jennings stocking mosquitofish concerns conservationists because & Hayes 1985). Possible mechanisms include habitat loss introduced mosquitofish can harm amphibians (e.g., or degradation, competition with and predation from the Woodward 1983; Gamradt & Kats 1996) and other native bullfrog (Rana catesbeiana), and predation by intro- species (Courtenay & Meffe 1989; Rupp 1996). Mosqui- duced fishes (Hayes & Jennings 1986). Some researchers tofish are capable of eliminating red-legged frog tadpoles have concluded that introduced predators are the most from simple communities in small artificial pools even likely cause of red-legged frog disappearance, although when tadpoles are as large or larger than the mosqui- multiple factors probably contribute to the decline (Hayes tofish (R. Schmeider & R. Nauman, personal communi- & Jennings 1986;